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The Fatty-Acid Hydratase Activity of the Most Common Probiotic Microorganisms

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The Fatty-Acid Hydratase Activity of the Most Common Probiotic Microorganisms catalysts Article The Fatty-Acid Hydratase Activity of the Most Common Probiotic Microorganisms Stefano Serra * , Davide De Simeis, Antonio Castagna and Mattia Valentino Consiglio Nazionale delle Ricerche (C.N.R.) Istituto di Scienze e Tecnologie Chimiche, Via Mancinelli 7, 20131 Milano, Italy; [email protected] (D.D.S.); [email protected] (A.C.); [email protected] (M.V.) * Correspondence: [email protected] or [email protected]; Tel.: +39-02-2399 3076 Received: 2 January 2020; Accepted: 23 January 2020; Published: 28 January 2020 Abstract: In this work, we studied the biotechnological potential of thirteen probiotic microorganisms currently used to improve human health. We discovered that the majority of the investigated bacteria are able to catalyze the hydration reaction of the unsaturated fatty acids (UFAs). We evaluated their biocatalytic activity toward the three most common vegetable UFAs, namely oleic, linoleic, and linolenic acids. The whole-cell biotransformation experiments were performed using a fatty acid concentration of 3 g/L in anaerobic conditions. Through these means, we assessed that the main part of the investigated strains catalyzed the hydration reaction of UFAs with very high regio- and stereoselectivity. Our biotransformation reactions afforded almost exclusively 10-hydroxy fatty acid derivatives with the single exception of Lactobacillus acidophilus ATCC SD5212, which converted linoleic acid in a mixture of 13-hydroxy and 10-hydroxy derivatives. Oleic, linoleic, and linolenic acids were transformed into (R)-10-hydroxystearic acid, (S)-(12Z)-10-hydroxy-octadecenoic, and (S)-(12Z,15Z)-10-hydroxy-octadecadienoic acids, respectively, usually with very high enantiomeric purity (ee > 95%). It is worth noting that the biocatalytic capabilities of the thirteen investigated strains may change considerably from each other, both in terms of activity, stereoselectivity, and transformation yields. Lactobacillus rhamnosus ATCC 53103 and Lactobacillus plantarum 299 V proved to be the most versatile, being able to efficiently and selectively hydrate all three investigated fatty acids. Keywords: probiotics; biocatalysis; hydratase; oleic acid; linoleic acid; linolenic acid; hydroxy fatty acids; stereoselective biotransformations; whole-cell processes 1. Introduction Probiotics are defined as live microorganisms intended to provide health benefits when administered in adequate amount, generally by improving or restoring the gut flora. Being regarded as beneficial for human health, they are included in the list of the GRAS microorganisms (Generally Recognized As Safe) and have gained increasing scientific and industrial relevance during the last few decades [1,2]. The growth of the probiotics market has fostered the biochemical studies of these species, especially those regarding the microorganism–human being interaction. Despite this fact, their use as biocatalysts for industrial biotransformation is restricted to a limited number of applications [3–12]. Among the most known probiotic bacteria, those belonging to the genus Lactobacillus and Bifidobacterium turned out to be the most promising for industrial purposes. In this context, the biotransformation 9 10 processes involving the D − double bond hydration of the C18 unsaturated fatty acids have received increasing attention. In fact, oleic, linoleic, and linolenic acid (Figure1) are the main components (as triglycerides) of the vegetable oils used for human consumption. Catalysts 2020, 10, 154; doi:10.3390/catal10020154 www.mdpi.com/journal/catalysts Catalysts 2020, 10, 154 2 of 18 Catalysts 2020, 10, 154 2 of 18 FigureFigure 1. 1.The The most most common common C C1818 unsaturatedunsaturated fatty acids: acids: oleic oleic (1 (),1 ),linoleic linoleic (2 (),2 and), and linolenic linolenic (3) (acid.3) acid. TheseThese fatty fatty acids acids share share inin commoncommon the presence of of a a ciscis doubledouble bond bond between between C(9) C(9) and and C(10) C(10) whosewhose hydration, hydration, in in principle, principle, cancan aaffordfford bothboth 9-hydroxy-fatty9-hydroxy-fatty acids acids (9-HFAs) (9-HFAs) and and 10-hydroxy-fatty 10-hydroxy-fatty acidacid (10-HFA) (10-HFA) derivatives. derivatives. AlthoughAlthough the aforementionedaforementioned positions positions of of the the fatty fatty acid acid chain chain possess possess veryvery similar similar chemical chemical reactivity,reactivity, the the main main part part ofof the the hydrating hydrating bacteria bacteria exclusively exclusively provides provides the 10- the 10-hydroxy-derivatives,hydroxy-derivatives, even even if the if the transformed transformed FAs FAscontain contain other other unsatu unsaturations.rations. In addition, In addition, this kind this kindof biotransformation of biotransformation is usually is usually very verystereose stereoselectivelective and a andsingle asingle enantiomer enantiomer is produced. is produced. ThisThis biochemical biochemical process process hashas beenbeen studiedstudied since the the early early 1960s 1960s [13], [13 ],but but the the class class of ofenzymes enzymes responsibleresponsible for for the the hydration hydration stepstep havehave beenbeen characterizedcharacterized only only recently recently [14]. [14 ].These These enzymes enzymes are are collectivelycollectively classified classified as as oleate oleate hydrataseshydratases (EC 4.2.1.53) and and have have received received growing growing attention attention both both fromfrom chemists chemists and and biologists biologists [ 15[15].]. AA numbernumber of putative putative oleate oleate hydratases hydratases have have been been identified identified from from bacteriabacteria including including di differentfferent probiotic probiotic strains, strains, and and then then isolated isolated andand characterizedcharacterized byby overexpression in heterologousin heterologous hosts hosts [16, 17[16,17].]. HFAs are important chemicals widely used for many industrial applications such as starting HFAs are important chemicals widely used for many industrial applications such as starting materials for biodegradable polymers, lubricants, emulsifiers, drugs, cosmetic ingredients, and materials for biodegradable polymers, lubricants, emulsifiers, drugs, cosmetic ingredients, and flavors [18–21]. It is worth noting that HFAs and some of their derivatives also possess relevant flavors [18–21]. It is worth noting that HFAs and some of their derivatives also possess relevant biological activities. A mixture of 10-HFAs was patented as an intestinal tract protecting agent [22] biological activities. A mixture of 10-HFAs was patented as an intestinal tract protecting agent [22] while while 10-hydroxystearic acid proved to ameliorate skin age spots and conspicuous pores [23]. Fatty 10-hydroxystearicacid esters of 13-hydroxy acid proved linoleic to ameliorate acid are skin anti-inflammatory age spots and conspicuous [24]: 9-hydroxystearic pores [23]. Fattyacid (9-HSA) acid esters ofshows 13-hydroxy anticancer linoleic properties acid are anti-inflammatory[25] whereas (12Z)-10-hydroxy-octadecenoic [24]: 9-hydroxystearic acid acid (9-HSA) possesses shows antifungal anticancer propertiesproperties [25 [26]] whereas and is (12 ableZ)-10-hydroxy-octadecenoic to prevent gastric Helicobacter acid possessesinfections antifungal by blocking properties their futalosine [26] and is ablepathways to prevent [27]. gastric In addition,Helicobacter recentinfections studies have by blockingdemonstrat theired futalosinethat HFAs pathwaysproduced [by27 ].human In addition, gut recentbacteria studies play have a relevant demonstrated role in the that control HFAs of produced allergy, inflammation, by human gut and bacteria immunity, play pointing a relevant to rolethe in theinvolvement control of allergy, of their inflammation, metabolites in andthe so-called immunity, gut–skin pointing axis to [28,29]. the involvement of their metabolites in the so-calledDespite gut–skin the general axis relevance [28,29]. of HFAs and the specific interest related to their effect on human health,Despite the hydratase the general activity relevance of the of probiotics HFAs and toward the specific the three interest most common related unsaturated to their effect fatty on acids human health,(UFAs) the 1– hydratase3 have been activity explored of the only probiotics marginally. toward More the threespecifically, most commonthe probiotics-mediated unsaturated fatty acidsbiotransformations (UFAs) 1–3 have of beenUFAs explored have been only tested, marginally. mainly using More oleic specifically, and linoleic the probiotics-mediatedacid as substrates, biotransformationswhereas a limited number of UFAs of have studies been have tested, examined mainly the usingbiotransformation oleic and linoleic of linolenic acid acid as substrates, [12,30]. whereasFurthermore, a limited the numberactivity of of the studies hydratases have has examined been investigated, the biotransformation mainly making of linolenicuse of recombinant acid [12,30 ]. Furthermore,hydratases and the thus activity employing of the hydratases isolated enzymes has been instead investigated, of studying mainly the fatty making acid biotransformation use of recombinant hydratasesin whole-cell and thusprocesses. employing This matter isolated is enzymesvery relevant instead as any of studying given probiotic the fatty microorganism acid biotransformation might inexpress whole-cell more processes. than a single This hydrat matterase isas very well relevantas
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